Calcium Intake Requirements Along the Life Cycle and Associated Factors

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Lorena Rubio-Navarro and Esther Perez-Torrero*

Division de Investigacion y Posgrado, Facultad de Ingenieria, Universidad Autonoma de Queretaro, Queretaro, Mexico

Abstract: Calcium is an essential nutrient required for various biological functions. Several studies have shown an association between calcium deficiencies and chronic diseases such as osteoporosis. The aim of this review was to collect relevant information about the importance of healthy bones, general requirements of calcium intake and special requirements during pregnancy and the lactation period. The risk of a fracture in elderly people is related to inadequate intake and metabolism of calcium during life that can affect the bone structure. In addition, some plant sources have high calcium content, proving the requirements of calcium especially to people with intolerance to common sources of calcium like milk. The effects of a balanced nutrition and physical activity during early life have long lasting beneficial effects in bone health in adulthood. Keywords: Bone, calcium requirements, food intake, life cycle, nutrition status, osteoporosis.

1. INTRODUCTION cells, fat and natural polymers such as polysaccharides, collagen type I and polyphosphates among other substances. The most abundant mineral in the human body is calcium While the properties of bone tissue and the proportions of the (Ca). Teeth and bones contain about 99% of the Ca in the substances vary with the different parts of the skeleton, in human body, while neurons, blood and other fluids contain general, the bone consists of two elements: mineral and or- the remaining one percent. The body needs Ca for muscles ganic. The mineral aspect constitutes 65-70% of its total and blood vessels to contract and expand, for the secretion of weight, composed principally of calcium phosphate orga- hormones and enzymes and to send messages through the nized in crystalline form, hydroxyapatite, calcium carbonate, nervous system. In early stages of development, the Ca in magnesium (Mg), sodium (Na), phosphorous (P) and fluo- ionic form can be used in different ways: as a cofactor of ride; 15-8% water; and 20-22% of organic matrix, which in some enzymes, or as an electrochemical agent, participating turn is composed mainly of collagen (90-96%). This relative in activation, permeability and stability of cell membranes; it proportion varies with age, site, gender, ethnic, disease and also acts as a second messenger in signal transduction in treatment [17, 18]. In terms of structure, bones can be con- muscle contraction and nerve transmission [1-3]. Maintain- sidered as a dispersion of mineral particles (biominerals) ing an adequate balance of Ca intake is necessary, since both embedded in an organic matrix, which forms the contiguous excess and deficiency have functional and metabolic impli- phase [4, 19, 20]. cations, and finally they determine adverse health effects. A reduction in consumption of Ca can cause neurological dis- The cellular components of bone are the osteogenic cells, orders such as tachycardia, convulsions and cardiovascular osteoblast, osteoclast, osteocytes and hematopoietic elements alterations [4], while hypocalcaemia may induce depression, [21]. There are different types of bones: woven bone is pre- psychosis, kidney stones, nausea, anorexia and others [5-7]. sent in the embryonic phase and in fractures (callous forma- Particularly, a Ca deficiency is related to other nutrient defi- tion); the cortical bone constitutes the principal structures of cits, mainly of vitamin A, vitamin D, iron and zinc [8-15]. the osteons, whose tight packing determines the mechanical Mineral Ca is lost through urine, sweat and feces [16] which strength of the cortical bone; the cancellous bone or trabecu- results in constant Ca loss from the bones, which must be lar bone represents the internal endosteal surfaces oriented replaced by that gained from food. In this review, we will perpendicular to external forces to provide structural support analyze the requirements of calcium and implicated factors and continually undergo remodeling [22]. by the human life cycle. 3. GENERAL REQUIREMENTS OF DIETARY 2. BONE COMPOSITION CALCIUM Bone and teeth tissue are the principal store of Ca. The The peak in bone density is at 25-30 years of age and is bones and teeth are living tissues composed of minerals, further affected by genetic factors, nutrition, physical activity and the endocrine system. This density is held at a steady state for around 10 years approximately, after which, a dis- *Address correspondence to this author at the Division de Investigacion y ruption between bone formation and bone desorption occurs. Posgrado, Facultad de Ingenieria, Universidad Autonoma de Queretaro, Cerro de las Campanas S/N, Queretaro, Qro., Mexico, CP 76010; Bone mass content depends on Ca intake throughout life, Tel: (52)442- 1921200. Ext. 65422; Fax: (52)442- 1921200. Ext. 6005; which must be appropriate from early stages of development E-mail: [email protected] until the adult age [23].

Ca recommendations vary between countries; many of milk are maintained at the expense of their health [55-57]. them fit the recommendations of other groups or countries Other studies have reported changes in Ca bone content, ab- having populations with some similarities [24-39]. In recent sorption, excretion and metabolism, but their causes are not years, countries with similar geographic characteristics have well known. It has been suggested that changes could be a been organizing committees to establish Ca recommenda- normal physiological response to the lack of Ca diet. The tions. For example, the European Community published nu- loss of mineral in bone that accompanies pregnancy and lac- tritional recommendations not only in Europe, but also in the tation may increase the risk of osteoporosis [58, 59]. U.S.A., Canada and Latin America. The reasons that make it The Ca supplementation intake for prophylaxis in preg- difficult to adjust the requirements between countries with nancy is in agreement with gastrointestinal tolerance, and similar populations are high costs, lack of financial and hu- pregnant women should get daily Ca during the second half man resources for nutritional studies, as well as global mar- of pregnancy, accompanied by other micronutrients. For this keting of junk foods [26]. reason, Ca citrate has advantages due to a lower rate of dys- It should be noted that the rate of absorption is inversely pepsia and flatulence, which ensures high efficacy rate in related to the amount provided in each serving, leading to the pregnant women. A regular intake of a micronutrient sup- recommendation of consumption of food rich in the mineral. plement at nutritional dose may be sufficient to supply and The recommendations for Ca intake are: for both sexes, 500 maintain the micronutrient levels of apparently healthy preg- mg/d for 1-3 years old, 800 mg/d for 4 to 8 years, for males nant women and could prevent low birth weight of newborns 9-13 years 1,100 mg/d, 14-18 years 1100 mg/d, 19-30 years [60, 61]. 800 mg/d, 31-50 years 800 mg/d 51-70years 800 mg/d and >70years 1000 mg/d for females 9-13 years 1,100 mg/d, 14- 5. CALCIUM SUPPLEMENTS LEAD TO 18 years 1100 mg/d, 19-30 years 800 mg/d, 31-50 years 800 PREGNANCY-INDUCED HYPERTENSION mg/d 51-70years 1000 mg/d and >70years 1000 mg/d for females [40]. At the age of 30, Ca consumption is higher During pregnancy, Ca metabolism is crossed by adapta- than it is excreted, which later starts to a decrease in the bone tions, mainly to compensate for the active flow of Ca to the density and surpass the stored Ca. The characteristic curve of fetus, which has increased from 50 mg/24 h at 20 weeks of bone mineral density shows that for both men and women, a gestation to 350 mg/24 h at 35 weeks of gestation. The fetus peak is observed at around 30 years of age, after which a accumulates a total of approximately 30 g of Ca at the end of decline in values follows. The excessive loss of Ca conduces the gestation period, of which 20 g are gained in the third to bone fragility and consequently, an increase in the risk of quarter. Moreover, the Ca balance is altered by the dilution fractures [26]. When the intake of mineral calcium is low in that produces the expansion of extracellular fluid volume, as the first 30 years of life, it is estimated that fracture risk may well as physiological hypercalciuria due to increased glome- be double later in life [41, 42]. Previous reports show that in rular filtration rate during pregnancy [62, 63]. teen ages, only about 25% individuals follow directions of Pregnancy-induced hypertension (PIH), is presented in appropriate Ca intake, while in adult population, only 50 or more than 10% of pregnant women, and is a risk factor for 60% reach the adequate intake [43, 44]. perinatal morbidity and mortality; additionally some risk factors include obesity before, and high weight gains during 4. REQUIREMENTS OF CALCIUM DURING pregnancy [62]. PIH is characterized by gestational hyper- PREGNANCY AND LACTATION tension, preeclampsia and eclampsia, which are responsible Calcium transfer from the mother to the fetus through the for morbidity and mortality and Ca supplementation may be placenta during pregnancy and lactation period is crucial for one factor in reducing the risk [33, 63]. The abnormal in- bone health of the both mother and the infant [45]. The re- crease in blood pressure usually develops after 20 weeks of quirements depend on the age of the mother: pregnancy age gestation, also presenting proteinuria and edema. The PIH of 14-18 years requires 1 000 mg/d calcium, 19-30 years can induce premature labor, resulting in low weight of the requires 800 mg/d and 31-50 years requires 800 mg/d; lacta- newborn [64]. The results of a study conducted in Ecuador tion period for 14-18 year old mothers requires 1 000 mg/d demonstrate that dietary Ca supplemented during pregnancy of Ca, for 19-30 years 800 mg/d of Ca is required and for 31- is safe and reduces the frequency of PIH in young women 50 years 800 mg/d Ca is required. During lactation, calcium with inadequate intake. Furthermore, the data suggest that losses into human breast milk represent 260 mg/L [46, 47]. supplementation of Ca and Vitamin D improved maternal The effects of this adaption in Ca metabolism show loss of and neonatal status [65], in addition to the Apgar scores in bone mineral density between 3.2-4.6% in trabecular area babies of mother receiving antenatal Vitamin D supplemen- [48, 49]. Previous reports show that during the first six tation [66]. Ca supplementation should be under strict con- months of the lactation period, there are temporal losses of trol to ensure that pregnant teenagers, whose bodies are still trabecular bone mineral at the spine and hip, of approxi- developing, have access to mineral dietary sources, with the mately 3-5 % [50]. aim of meeting the demands of their own growth and ensur- ing the proper progress of pregnancy and the development of Deficiency in mineral Ca intake during pregnancy in- the child [64, 67-69]. Moreover, additional strategies that can duces abnormal bone fetal programming that delays fetal be used to reduce hypertension include maintaining healthy growth [51]; the requirements are based on the individual body weight through diet and exercise, reduced sodium in- differences between women, during pregnancy. There is sub- take, and lower alcohol intake [70]. stantial evidence that maternal nutritional status interferes with the bone mass of their progeny [52-54]. Even in the The mechanism, by which Ca and sodium affect blood case of undernourished mothers, the quantity and quality of pressure, is by altering certain regulatory systems. In the case 72 Current Nutrition & Food Science, 2015, Vol. 11, No. 1 Rubio-Navarro and Perez-Torrero of sodium, the renin-aldosterone system and in the case of in trabecular and cortical zones [85]. In osteoporosis, the Ca, vitamin D and others are affected. These hormones in spongy bone is characterized by a loss of architectural struc- turn regulate the cytosolic free Ca, which participates as a tures, particularly the trabecular with less density in this area, second messenger in various reactions. A high level of free increase in cavities and decrease in the number of trabeculae Ca in the cytoplasm increases smooth muscle contraction, in the proximal femur, which in older ages is difficult to be secretion of catecholamine, central nervous system activity replaced and consequently becomes more fragile and suscep- and thus increases blood pressure. A high Ca intake de- tible to rupture. One of the current problems facing the creased in the cytoplasm due to vitamin D, keeping the blood health professional is to make a correct diagnosis, for deter- pressure maintained [71]. mination of a response to the treatment administered. Moreover, an increase in Ca intake requirement daily in men 6. OSTEOPOROSIS and postmenopausal women can be an option to reduce the bone loss related to age [83, 84]. Osteoporosis was defined in 1991 as a bone systemic disease, characterized by loss of bone density, mass and loss of 7. NUTRITIONAL STATUS microarchitecture of the bone tissue, which causes bone fragility with enhanced risk of fracture. The risk of osteoporosis Nutritional status is only one of the many factors that in- is determined by genetic factors, a sedentary lifestyle (lack fluence bone mass and the likelihood of facture but it is par- of exercise), high weight, smoking and drinking alcohol ticularly interesting because it is modifiable, unlike other among other factors [72]. The beginning of osteoporosis may factors (Romero and Rivas, 2014). A balanced diet with an be due to loss of bone mineral consequently making the adequate intake of calories and nutrients is essential for the bones more vulnerable to breakage. The bone loss is fre- development of all tissues, including bone. However, not all quently associated to aging process, usually beginning be- individuals follow an optimal diet for bone health [43]. Nu- tween the ages of 35 and 40 years, leading to a shrinking of tritional deficiencies in the diet affect changes in bone min- the skeleton. Postmenopausal women are at high risk of os- eral density and adversely affect optimal functionality. Mal- teoporosis because of estrogen deficiencies [73, 74]. nutrition is one of the environmental factors that cause adverse effects on the optimal development of the individual by Based on the measurement of bone mineral density, it is altering the morphological and functional development nerv- estimated that 30% of postmenopausal Caucasian women (> ous system [86, 87, 91] and the behavioral patterning [92, 50 years) have osteoporosis, the disease which progresses 93]. silently and painlessly until a fracture occurs, most often occurring in the hip, spine and wrist [75, 76]. The WHO has The effects depend on the period in which malnutrition is classified the diagnosis based on the measurement of mineral installed, although it is known that an organism exposed to bone density [6]. Osteoporosis is the most common cause of malnutrition presents certain coping mechanisms to survive, fractures at 45 years of age, affecting 20% of postmeno- and these changes remain in the long-term and predispose pausal women, approximately 7.8 million in the word with the body to a number of adverse physiological changes in the prediction for 2040 being three times more. The risk of a adulthood. Nutritional deficiencies of some elements such as fracture for 50 year old women and men is 40% and 13 %, vitamins, minerals, proteins, carbohydrates and lipids, result respectively. in functional changes at the cellular level, and these conditions can cause alterations in the bone mineralization The most important consequence of osteoporosis is lim- [94, 95]. ited mobility of the individual, causing the loss of personal independence and an impaired quality of life, as well as large Calcium (Ca) and phosphorus (P) are the main mineral economic consequences [77]. The disease occurs at a rate components of the bone, as they compose roughly 80 to 90% four times higher in women than men. In men, osteoporosis of the mineral content of bone. Protein is essential because it is considered to result from factors related to age, whereas in is incorporated into the organic matrix of bone for collagen women, it is related to hormonal fluctuations [78]. Currently, structures upon which mineralization occurs; trace elements there is a growing recognition that osteoporosis and fractures and vitamins (Vit. D and K) are also crucial in carrying out in men are a significant public global health problem and metabolic processes and reactions in the bone [96-100]; on increase with age [79], possibly due to declining sex steroid the other hand, phytochemicals, antioxidants and other bio- levels like testosterone and other hormonal changes but there active compounds influence bone metabolism basically by is little available long-term data [80, 81]. It is important to reducing oxidative stress and inflammation processes [101]. note that the mineralized bone mass is a dynamic, living tis- Both the minerals Ca and P are essential for the function sue modified constantly by a process of removal of old mate- and structure of tissues, just as their physiology and metabo- rial and replacement with new [75, 76, 82-84]. In the early lism are regulated and interrelated by other dietary factors stages of development, more bone is removed, reaching the such as parathyroid hormone and vitamin D. The joint activ- highest density and bone strength in adolescence, which is ity of these nutritional factors is involved in the regulation followed by the adulthood stage during which old bone is and homeostasis of P and Ca [102, 103]. Ca and P should be removed at a rate greater than that which can be replaced, available simultaneously and in sufficient quantities for ade- leading to a loss of mineral content. quate bone mineralization. The lack of these minerals causes The postmenopausal period is associated with estrogen osteopenia, rickets and increases the risk of fractures deficiency, because the ovaries produce less estrogen. The [104, 105]. effects of this deficiency alter the dynamics of bone tissue, Phosphorous (P) in combination with ion provides increasing the activation frequency of new remodeling sites strength to bones and teeth [98, 106]. Therefore, although the Calcium Intake Requirements along the Life Cycle and Associated Factors Current Nutrition & Food Science, 2015, Vol. 11, No. 1 73 concentration of Ca is adequate according to intake recom- such as the regime of 1,600 calories or less, do not provide mendations, demineralization can occur when it is dispropor- adequate amounts of Ca, and over long periods of time result tionate in their content [106, 107]. The P deficient diet inter- in its deficiency. Ca is found in a wide variety of foods such feres with the mineralization process, leading to osteoblast as dairy products, green leafy vegetables, nuts and seeds dysfunction. The P deficiency is related to low intake in the (almonds, sesame seeds) and fortified flour with calcium diet, especially in individuals who are treated with antacids carbonate, in Latin America and the Caribbean [119]. The that bind to P, leading to a decrease in bone mass [108]. On main source of Ca is milk and dairy products, but when the the other hand, vitamin D deficiency hypophosphatemia is consumption of these foods is limited, there are other associated with metabolic acidosis, which induces mobiliza- sources, including fish with edible bones, nixtamalized tortil- tion of hydroxyapatite from bones [8, 108, 109]. This proc- las, broccoli, cabbage, legumes, tofu and prickly pads among ess is associated with hypercalciuria; the removal of hy- others [120-122]. Ca supplements are also a recommended droxyapatite carbonate ions releases a dampening effect on source, when not getting enough through diet. Supplements the retention of hydrogen ions in serum. To treat this condi- containing calcium carbonate have the highest percentage of tion, milk intake is recommended because milk contains 100 elemental Ca, which is absorbed by the body easily [123]. mg/dl of P or sodium phosphate or potassium phosphate The contribution of Ca in plant foods is important, when [110]. the food dependence of many populations in the world is mainly on plants, as in rural areas in countries like Mexico, 8. EXERCISE AND OSTEOPOROSIS PREVENTION where tortillas and cactus are a major source of this mineral. Exercise is essential to preserve and maintain adequate In Mexico, corn products are prepared in several ways, in- bone mass and is encouraged to maintain or increase muscle cluding boiled or roasted corn, popcorn, corn soup, pozole, strength, coordination and balance to help prevent bone frac- gravies, champurrado, tamales and most importantly, the tures. The main benefit is obtained by regular physical exer- tortilla. The preparation of the tortilla dough is traditionally cise in adolescence, before reaching the peak bone mass; the through the alkaline cooking process and is consumed as future risk of fracture decreases with the maximum peak memelas, tacos, tlacoyos, chips, fat, soups, peneque, and bone mass [111, 112]. Some research shows that physical tamales to name a few. Mostly rural consumption of tortilla activity with weights has beneficial effect in healthy bones at is up to 67% of the total energy consumed by the Mexican any age. Physical activity at high intensity of forces like population [124]. plyometric exercises, gymnastics and high intensity resis- The addition of lime in the alkaline cooking process of tance training can increase the bone mass in young and ado- corn increases the total concentration of Ca, which is ab- lescents. In rodent models, the osteogenic responses to me- sorbed through the diet and at the same time, is a function of chanical tension are maximized by dynamic charge of forces the number of tortillas consumed [125]. The processing of that produce high tension; however, this and other results corn with lime enhances the Ca content from 0.07% (un- show that the beneficial affects by exercises in children and treated corn content) to 0.5% in boiled products [126]. In the young have long lasting beneficial effect until adulthood. case of intake of tortilla, per capita of 326 grams and levels This outlines the necessity of physical activity in early de- of 0.30% in a dry form are the main sources of this mineral velopment for bone health [113, 114]. in all populations in Mexico and it basically meets 75% of Currently, we do not have a program specific to each pe- daily requirements; therefore, it holds great importance and riod of life but research has shown that there are two types of should not be removed from the diet. exercises beneficial to bone mineral density, these are: 1) The plant of genus Opuntia (cactus) is considered an im- strength training, particularly weight lifting, and 2) exercise portant source of food around world including Mexico, of muscles and bones working against gravity, in which arms Chile, and Italy, and is used for commercial purposes in and legs are weight-bearing (walking, stair climbing, run- various regions of the United States of America (USA) ning, dancing, hiking, gymnastics, soccer, swimming, cy- [127]. Another reason for which this cactus plant is included cling etc.). Experts recommend an exercise program for 30 in the diet is because it has been considered as an important minutes a day, 5 to 6 days a week, maintaining a high level source with nutritional and medicinal value based on its nu- of daily activity according to age, lifestyle, strength and trient composition. lightness of each individual [43]. Recent studies have shown that the Ca content in cactus 9. SOURCE OF CA is elevated, reaching higher values compared to other vegetables. In addition, we found that the Ca content of the nopal In recent years, we have studied the availability of Ca in in a dry form depends on the state of maturation. In the regional food, being aware of the importance of quantifying young cactus, the content is 1.54% whereas in mature cactus the intake of this mineral through diet. Nonetheless, the (stalk), it is 4.15%. Considering that this product is popular, availability of Ca-rich foods does not ensure their consump- its consumption could thus contribute significantly to the tion, due to different influencing factors such as customs, optimal values of Ca required for good health. Dehydrated economics and personal taste, among others. prickly pads at advanced degree of maturity can be an alter- Currently, research is focused to study the strategies to native source of calcium and fiber [128]. In a comparative eliminate these deficiencies of Ca, for example, by improv- study on the disposition of minerals in plants, an analysis ing the bioavailability of minerals in legumes and other was made in the prickly pears, spinach and kale obtained plants like cactus included in groceries and food for grazing from the market, the data showed that plants are rich in vari- animals [115-118]. Intense diets intended for weight loss, ous minerals, with the cactus found to contain the highest 74 Current Nutrition & Food Science, 2015, Vol. 11, No. 1 Rubio-Navarro and Perez-Torrero amount of Ca. This fact highlights the potential usefulness of consumption of Ca throughout life will help design models the cactus as a source of Ca for individuals who are intoler- of adequate diets for different stages of life, based on the ant to lactose in adulthood, leading to a drastic reduction in knowledge of other factors that determine their absorption. dairy foods that carries digestive disorders, as a greater intol- The factors involved in the development of diseases re- erance to lactose has been associated in osteoporotic indi- lated to genesis of osteoporosis are: a low intake of Ca dur- viduals than in healthy people [128-130]. ing life is extensively associated to nutritional conditions, poor absorption of Ca, a sedentary lifestyle, prolonged im- 10. CALCIUM ABSORPTION mobilization and extreme thinness. The main measure in the The process of absorption of Ca is more efficient in an treatment of osteoporosis prevention is based on diet and acid medium; the majority of Ca absorption occurs in the healthy lifestyle and is considered the only effective meas- upper of the duodenum and absorbs only 20-30% of Ca ure, because once softening occurs, it is difficult to reverse intake. In order to increase the intake of Ca, it should be the damage [139]. Whenever possible, Ca must be obtained noted that there are dietary components that contribute to from natural sources in the diet [140]. Although supplements increase or decrease in its absorption [131]. Among the fac- may be administered to children who do not get enough Ca tors that favor absorption is vitamin D, which regulates the in foods consumed daily, mineral Ca is a vital mineral stor- movement of Ca in and out of the bone. Improved absorption age in the bone, which plays a role in cell physiology in or- of Ca in the intestine, also involved in the mineralization of der to maintain vascular tone, as a regulatory factor to pre- the osteoclast, increases the secretion of osteocalcin and vent adverse health effects. The body's nutritional status is a phosphatidyl serine. Lactose increases the intestinal absorp- factor, both for developing and prevention of deficient nu- tion, or may be an obstruction in people with lactase defi- trimental associated diseases. ciency. Zinc influences the transport of Ca through the intestinal lining. Consumption of carbonated drinks like sodas CONFLICT OF INTEREST decreases the absorption of Ca. The authors confirm that this article content has no con- Oxalates and phytates, which form complexes with Ca in flict of interest. the small intestine, block its absorption [132]. Phytates are on the outside of the shell of cereals such as oats, but are ACKNOWLEDGEMENTS destroyed when the grain is fermented with yeast. Another important factor to consider is the Ca/P, because it has been The study was partly supported by the National Council suggested that diets high in P or having inadequate Ca/P lead of Science and Technology México (CONACyT) for Post- to secondary hyperparathyroidism and an increase in Ca in doctoral Fellow to LR No. 4159641596 and Research Sup- the urine and increased bone loss [133]; it is therefore rec- port Program of National University of Queretaro (FOFI- ommended to maintain 1:1.3 relation ratios. Moreover, high UAQ 2013) Grant FN-2014-19 EPT. The authors would also protein intake promotes hypercalciuria by oxidation of ex- like to acknowledge Agustin Esparza for editing the English cess methionine and cysteine of hyper protein diets [134]. content of this document. 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Received: October 09, 2014 Revised: November 25, 2014 Accepted: December 06, 2014

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